Abstract
Symbiodiniaceae is a diverse group of dinoflagellates that form symbioses with marine invertebrates, provisioning energy and nutrients for their hosts. Symbiont diversity is a well-known predictor of host fitness and stress tolerance. Yet, we have a limited understanding of the mechanisms by which in hospite symbiont communities are structured. Therefore, we hypothesized that phylogenetic differences in nitrogen assimilation may affect symbiont dominance, as has been demonstrated in phytoplankton communities. Here, we quantified species-specific rates of nitrate assimilation using stable isotope labeling, and investigated key traits that have been adopted in phytoplankton ecology to explain the fundamental concept of nitrogen acquisition strategies and size-related trade-offs in Symbiodiniaceae. Traits related to structure and function were measured to look for convergent ecological strategies. Despite the limited sample size, we could distinguish two groups among the five species of Symbiodiniaceae with features described by the phytoplankton’s competition theories for resources: the affinity-adapted species which were associated with larger size, higher nitrogen content and nitrate affinity; and the velocity-adapted species which were small size, efficient in maximum nitrate assimilation, specific carbon assimilation rate, and growth. Our work supports the relevance of a functional trait-based approach to describe Symbiodinaceae diversity. The two contrasting nitrogen acquisition strategies identified may be fundamental to explain the composition and dynamics of Symbiodinaceae in hospite, stressing the importance of bottom-up mechanisms in shaping symbiont composition.
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27 January 2021
A Correction to this paper has been published: https://doi.org/10.1007/s00338-021-02063-4
References
Adler PB, Salguero-Gómez R, Compagnoni A, Hsu JS, Ray-Mukherjee J, Mbeau-Ache C, Franco M (2014) Functional traits explain variation in plant life history strategies. PNAS 111(2):740–745
Aksnes DL, Egge JK (1991) A theoretical model for nutrient uptake in phytoplankton. Mar Ecol Prog Ser 70(1):65–72
Amarasekare P, Coutinho RM (2014) Effects of temperature on intraspecific competition in ectotherms. Am Nat 184:E50–65
Anderson SL, Burris JE (1987) Role of glutamine synthetase in ammonia assimilation by symbiotic marine dinoflagellates (zooxanthellae). Mar Biol 94(3):451–458
Baker AC, Starger CJ, McClanahan TR, Glynn PW (2004) Corals’ adaptive response to climate change. Nature 430(7001):741–741
Baker DM, Andras JP, Jordán-Garza AG, Fogel ML (2013) Nitrate competition in a coral symbiosis varies with temperature among Symbiodinium clades. ISME J 7(6):1248–1251
Baker DM, Freeman CJ, Wong JCY, Fogel ML, Knowlton N (2018) Climate change promotes parasitism in a coral symbiosis. ISME J 12(3):921–930
Barott KL, Venn AA, Perez SO, Tambutté S, Tresguerres M (2015) Coral host cells acidify symbiotic algal microenvironment to promote photosynthesis. Proc Natl Acad Sci 112(2):607–612
Biquand E, Okubo N, Aihara Y, Rolland V, Hayward DC, Hatta M, Minagawa J, Maruyama T, Takahashi S (2017) Acceptable symbiont cell size differs among cnidarian species and may limit symbiont diversity. ISME J 11(7):1702–1712
Bonachela JA, Raghib M, Levin SA (2011) Dynamic model of flexible phytoplankton nutrient uptake. Proc Natl Acad Sci 108(51):20633–20638
Boulotte NM, Dalton SJ, Carroll AG, Harrison PL, Putnam HM, Peplow LM, van Oppen MJH (2016) Exploring the Symbiodinium rare biosphere provides evidence for symbiont switching in reef-building corals. ISME J 10(11):2693–2701
Browne NK, Tay JKL, Low J, Larson O, Todd PA (2015) Fluctuations in coral health of four common inshore reef corals in response to seasonal and anthropogenic changes in water quality. Mar Environ Res 105:39–52
Camp EF, Edmondson J, Doheny A, Rumney J, Grima AJ, Huete A, Suggett DJ (2019) Mangrove lagoons of the Great Barrier Reef support coral populations persisting under extreme environmental conditions. Mar Ecol Prog Ser 625:1–14
Cantin NE, van Oppen MJH, Willis BL, Mieog JC, Negri AP (2009) Juvenile corals can acquire more carbon from high-performance algal symbionts. Coral Reefs 28(2):405–414
Chang SS, Prézelin BB, Trench RK (1983) Mechanisms of photoadaptation in three strains of the symbiotic dinoflagellate Symbiodinium microadriaticum. Mar Biol 76(3):219–229
Conti-Jerpe IE, Thompson PD, Wong CWM, Oliveira NL, Duprey NN, Moynihan MA, Baker DM (2020) Trophic strategy and bleaching resistance in reef-building corals. Sci Adv 6(15):eaaz5443
Corcoran AA, Boeing WJ (2012) Biodiversity increases the productivity and stability of phytoplankton communities. PLoS ONE 7(11):1–9
Crossland CJ, Barnes DJ (1974) The role of metabolic nitrogen in coral calcification. Mar Biol 28(4):325–332
Crowley PH (1975) Natural selection and the Michaelis constant. J Theor Biol 50(2):461–475
D’Elia CF, Domotor SL, Webb KL (1983) Nutrient uptake kinetics of freshly isolated zooxanthellae. Mar Biol 75(2–3):157–167
Dortch Q, Clayton JR, Thoresen SS, Ahmed SI (1984) Species differences in accumulation of nitrogen pools in phytoplankton. Mar Biol 81(3):237–250
Dugdale RC, Wilkerson FP (1986) The use of 15N to measure nitrogen uptake in eutrophic oceans; experimental consideration. Limnol Oceanogr Ocean 31(4):673–689
Duysens LNM (1956) The flattening of the absorption spectrum of suspensions, as compared to that of solutions. Biochim Biophys Acta 19:1–12
Edwards KF, Thomas MK, Klausmeier CA, Litchman E (2012) Allometric scaling and taxonomic variation in nutrient utilization traits and maximum growth rate of phytoplankton. Limnol Oceanogr 57(2):554–566
Enríquez S, Agustí S, Duarte CM (1994) Light absorption by marine macrophytes. Oecologia 98(2):121–129
Enríquez S, Duarte CM, Sand-Jensen K, Nielsen SL (1996) Broad-scale comparison of photosynthetic rates across phototrophic organisms. Oecologia 108(2):197–206
Enríquez S, Méndez ER, Hoegh-Guldberg O, Iglesias-Prieto R (2017) Key functional role of the optical properties of coral skeletons in coral ecology and evolution. Proc R Soc B 284(1853):20161667
Enríquez S, Méndez ER, Iglesias-Prieto R (2005) Multiple scattering on coral skeletons enhances light absorption by symbiotic algae. Limnol Ocean 50(4):1025–1032
Eppley RW, Coatsworth JL, Solorzano L (1969) Studies of nitrate reductase in marine phytoplankton. Limnol Oceanogr 14(2):194–205
Fiksen Ø, Follows MJ, Aksnes DL (2013) Trait-based models of nutrient uptake in microbes extend the Michaelis-Menten framework. Limnol Oceanogr 58(1):193–202
Finkel ZV, Beardall J, Flynn KJ, Quigg A, Rees TAV, Raven JA (2010) Phytoplankton in a changing world: cell size and elemental stoichiometry. J Plankton Res 32(1):119–137
Flynn KJ (1998) Estimation of kinetic parameters for the transport of nitrate and ammonium into marine phytoplankton. Mar Ecol Prog Ser 169:13–28
Flynn KJ (2003) Modelling multi-nutrient interactions in phytoplankton; balancing simplicity and realism. Prog Oceanogr 56(2):249–279
Flynn KJ, Skibinski DOF, Lindemann C (2018) Effects of growth rate, cell size, motion, and elemental stoichiometry on nutrient transport kinetics. PLoS Comput Biol 14(4):e1006118
Follows MJ, Dutkiewicz S, Grant S, Chisholm SW. Emergent biogeography of microbial communities in a model ocean. Science 315(5820):1843–1846
Geider R, Piatt T, Raven J (1986) Size dependence of growth and photosynthesis in diatoms: a synthesis. Mar Ecol Prog Ser 30:93–104
Geider RJ, Osborne BA (1987) Light absorption by a marine diatom: experimental observations and theoretical calculations of the package effect in a small Thalassiosira species. Mar Biol 96(2):299–308
Geider RJ, La Roche J, Greene RM, Olaizola M (1993) Response of the photosynthetic apparatus of Phaeodactylum tricornutum (Bacillariophyceae) to nitrate, phosphate, or iron starvation. J Phycol 29(6):755–766
Gilbert PM, Lipschultz F, Mccarthy JJ, Altabet MA (1982) Isotope dilution models of uptake and remineralization of ammonium by marine plankton. Limnol Oceanogr 27(4):639–650
Goyen S, Pernice M, Szabó M, Warner ME, Ralph PJ, Suggett DJ (2017) A molecular physiology basis for functional diversity of hydrogen peroxide production amongst Symbiodinium spp. (Dinophyceae). Mar Biol 164(3):1–12
Gunnersen J, Yellowlees D, Miller DJ (1988) The ammonium/methylammonium uptake system of Symbiodinium microadriaticum. Mar Biol 97(4):593–596
Hatcher BG (1988) Coral reef primary productivity: a beggar’s banquet. Trends Ecol Evol 3(5):106–111
Hayes JM (1983) Practice and principles of isotopic measurements in organic geochemistry. Organic geochemistry of contemporaneous and ancient sediments 5:e5
Hein M, Pedersen MF, Sand Jensen K (1995) Size-dependent nitrogen uptake in micro- and macroalgae. Mar Ecol Prog Ser 118(1):247–254
Hoogenboom M, Beraud E, Ferrier-Pagès C (2010) Relationship between symbiont density and photosynthetic carbon acquisition in the temperate coral Cladocora caespitosa. Coral Reefs 29(1):21–29
Hu S, Smith WO (1998) The effects of irradiance on nitrate uptake and dissolved organic nitrogen release by phytoplankton in the Ross Sea. Cont Shelf Res 18(9):971–990
Hughes AD, Grottoli AG (2013) Heterotrophic compensation: a possible mechanism for resilience of coral reefs to global warming or a sign of prolonged stress? PLoS ONE 8:e81172
Hughes DJ, Varkey D, Doblin MA, Ingleton T, Mcinnes A, Ralph PJ, van Dongen-Vogels V, Suggett DJ (2018) Impact of nitrogen availability upon the electron requirement for carbon fixation in Australian coastal phytoplankton communities. Limnol Oceanogr 63(5):1891–1910
Iglesias-Prieto R, Trench RK (1994) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser 113(1):163–176
Iglesias-Prieto R, Trench RK (1997) Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll–protein complexes to different photon-flux densities. Mar Biol 130(1):23–33
Jackson AE, Yellowlees D (1990) Phosphate uptake by zooxanthellae isolated from corals. Proc R Soc Lond Ser B Biol Sci 242(1305):201–204
Joint IR, Pomroy AJ (1988) Allometric estimation of the productivity of phytoplankton assemblages. Mar Ecol Prog Ser 47(2):161–168
Junk GA, Svec HJ (1958) Nitrogen isotope abundance measurements. Ames Lab ISC Tech Reports ISC-1138:1–37
Key T, McCarthy A, Campbell DA, Six C, Roy S, Finkel ZV (2010) Cell size trade-offs govern light exploitation strategies in marine phytoplankton. Environ Microbiol 12(1):95–104
Kimes NE, Johnson WR, Torralba M, Nelson KE, Weil E, Morris PJ (2013) The Montastraea faveolata microbiome: ecological and temporal influences on a Caribbean reef-building coral in decline. Environ Microbiol 15(7):2082–2094
Kirk JTO (1994) Light and photosynthesis in aquatic ecosystems. Cambridge University Press, Cambridge
Kolber Z, Zehr J, Falkowski P (1988) Effects of growth irradiance and nitrogen limitation on photosynthetic energy conversion in photosystem II. Plant Physiol 88(3):923–929
Kraft NJ, Godoy O, Levine JM (2015) Plant functional traits and the multidimensional nature of species coexistence. Proc Natl Acad Sci 112(3):797–802
Krueger T, Horwitz N, Bodin J, Giovani M, Escrig S, Fine M, Meibom A, Krueger T (2020) Intracellular competition for nitrogen controls dinoflagellate population density in corals. Proc R Soc B 287(1922):20200049
LaJeunesse TC (2001) Investigating the biodiversity, ecology, and phylogeny of endosymbiotic dinoflagellates in the genus Symbiodinium using the ITS region: in search of a “species” level marker. J Phycol 37(5):866–880
LaJeunesse T (2002) Diversity and community structure of symbiotic dinoflagellates from Caribbean coral reefs. Mar Biol 141(2):387–400
LaJeunesse TC, Lambert G, Andersen RA, Coffroth MA, Galbraith DW (2005) Symbiodinium (Pyrrhophyta) genome sizes (DNA content) are smallest among dinoflagellates. J Phycol 41(4):880–886
LaJeunesse TC, Lee SY, Gil-Agudelo DL, Knowlton N, Jeong HJ (2015) Symbiodinium necroappetens sp. nov. (Dinophyceae): sn opportunist ‘zooxanthella’ found in bleached and diseased tissues of Caribbean reef corals. Eur J Phycol 50(2):223–238
LaJeunesse TC, Pettay DT, Sampayo EM, Phongsuwan N, Brown B, Obura DO, Hoegh-Guldberg O, Fitt WK (2010) Long-standing environmental conditions, geographic isolation and host-symbiont specificity influence the relative ecological dominance and genetic diversification of coral endosymbionts in the genus Symbiodinium. J Biogeogr 37(5):785–800
LaJeunesse TC, Wham DC, Pettay DT, Parkinson JE, Keshavmurthy S, Chen CA (2014) Ecologically differentiated stress-tolerant endosymbionts in the dinoflagellate genus Symbiodinium (Dinophyceae) clade D are different species. Phycologia 53(4):305–319
Laurion I, Vincent WF (1998) Cell size versus taxonomic composition as determinants of UV-sensitivity in natural phytoplankton communities. Limnol Oceanogr 43(8):1774–1779
Lawson CA, Possell M, Seymour JR, Raina JB, Suggett DJ (2019) Coral endosymbionts (Symbiodiniaceae) emit species-specific volatilomes that shift when exposed to thermal stress. Sci Rep 9(1):1–11
Lawson CA, Raina JB, Kahlke T, Seymour JR, Suggett DJ (2018) Defining the core microbiome of the symbiotic dinoflagellate, Symbiodinium. Environ Microbiol Rep 10(1):7–11
Lee MJ, Jeong HJ, Jang SH, Lee SY, Kang NS (2016) Most low-abundance “background” Symbiodinium spp. are transitory and have minimal functional significance for symbiotic corals. Microb Ecol 71(3):771–783
Legendre P, Legendre L (2012) Numerical Ecology. Elsevier, Amsterdam
Levine JM (2016) Ecology: a trail map for trait-based studies. Nature 529(7585):163–164
Lin S, Zhang Y, Zhang H, Ji Z, Cai M, Zhuang Y (2015) The Symbiodinium kawagutii genome illuminates dinoflagellate gene expression and coral symbiosis. Science 350(6261):691–694
Lindemann C, Fiksen Ø, Andersen KH, Aksnes DL (2016) Scaling laws in phytoplankton nutrient uptake affinity. Front Mar Sci 3:26
Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Annu Rev Ecol Evol Syst 39:615–639
Litchman E, Klausmeier CA, Schofield OM, Falkowski PG (2007) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecol Lett 10(12):1170–1181
Lomas MW, Gilbert PM (2000) Comparisons of nitrate uptake, storage, and reduction in marine diatoms and flagellates. J Phycol 36(5):903–913
Mcgill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21(4):178–185
McIlroy SE, Wong JCY, Baker DM (2020) Competitive traits of coral symbionts may alter the structure and function of the microbiome. ISME J 14:2424–2432
Morel A, Bricaud A (1981) Theoretical results concerning light absorption in a discrete medium, and application to specific absorption of phytoplankton. Deep Sea Res Part A Oceanogr Res Pap 28(11):1375–1393
Morris LA, Voolstra CR, Quigley KM, Bourne DG, Bay LK (2019) Nutrient availability and metabolism affect the stability of coral–Symbiodiniaceae symbioses. Trends Microbiol 27(8):678–689
Muscatine L, Porter JW (1977) Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience 27(7):454–460
Niklas KJ (1994) The scaling of plant and animal body mass, length, and diameter. Evolution 48(1):44–54
Parkinson JE, Baums IB (2014) The extended phenotypes of marine symbioses: ecological and evolutionary consequences of intraspecific genetic diversity in coral-algal associations. Front Microbiol 5:445
Pernice M, Dunn SR, Tonk L, Dove S, Domart-Coulon I, Hoppe P, Schintlmeister A, Wagner M, Meibom A (2015) A nanoscale secondary ion mass spectrometry study of dinoflagellate functional diversity in reef-building corals. Environ Microbiol 17(10):3570–3580
Pochon X, Pawlowski J, Zaninetti L, Rowan R (2001) High genetic diversity and relative specificity among Symbiodinium-like endosymbiotic dinoflagellates in soritid foraminiferans. Mar Biol 139(6):1069–1078
Rädecker N, Raina J-B, Pernice M, Perna G, Guagliardo P, Kilburn MR, Aranda M, Voolstra CR (2018) Using Aiptasia as a model to study metabolic interations in Cnidarian-Symbiodinium symbioses. Front Physiol 9:214
Raven JA, Finkel ZV, Irwin AJ (2005) Picophytoplankton: bottom-up and top-down controls on ecology and evolution. Vie milieu 55(3-4):209–215
Reynolds CS (1984) Phytoplankton periodicity: the interactions of form, function and environmental variability. Freshw Biol 14(2):111–142
Rodriguez-Lanetty M, Chang SJ, Song JI (2003) Specificity of two temperate dinoflagellate-anthozoan associations from the north-western Pacific Ocean. Mar Biol 143(6):1193–1199
Ros M, Camp EF, Hughes DJ, Crosswell JR, Warner ME, Leggat WP, Suggett DJ (2020) Unlocking the black-box of inorganic carbon-uptake and utilization strategies among coral endosymbionts (Symbiodiniaceae). Limnol Oceanogr 65(8):1747–1763
Scheufen T, Iglesias-Prieto R, Enríquez S (2017a) Changes in the number of symbionts and Symbiodinium cell pigmentation modulate differentially coral light absorption and photosynthetic performance. Front Mar Sci 4:309
Scheufen T, Krämer WE, Iglesias-Prieto R, Enríquez S (2017b) Seasonal variation modulates coral sensibility to heat-stress and explains annual changes in coral productivity. Sci Rep 7(1):1–15
Smith SL, Yamanaka Y (2007) Optimization-based model of multinutrient uptake kinetics. Limnol Oceanogr 52(4):1545–1558
Smith SL, Yamanaka Y, Pahlow M, Oschlies A (2009) Optimal uptake kinetics: Physiological acclimation explains the pattern of nitrate uptake by phytoplankton in the ocean. Mar Ecol Prog Ser 384:1–12
Sommer U (1991) A comparison of the Droop and the Monod models of nutrient limited growth applied to natural populations of phytoplankton. Funct Ecol 5:535–544
Sommer U (1984) The paradox of the plankton: fluctuations of phosphorus availability maintain diversity of phytoplankton in flow-through cultures. Limnol Ocean 29(3):633–636
Sproles AE, Kirk NL, Kitchen SA, Oakley CA, Grossman AR, Weis VM, Davy SK (2018) Phylogenetic characterization of transporter proteins in the cnidarian-dinoflagellate symbiosis. Mol Phylogenet Evol 120:307–320
Stolte W, Riegman R (1995) Effect of phytoplankton cell size on transient-state nitrate and ammonium uptake kinetics. Microbiology 141(5):1221–1229
Suggett DJ, Goyen S, Evenhuis C, Szabó M, Pettay DT, Warner ME, Ralph PJ (2015) Functional diversity of photobiological traits within the genus Symbiodinium appears to be governed by the interaction of cell size with cladal designation. New Phytol 208(2):370–381
Suggett DJ, Warner ME, Leggat W (2017) Symbiotic dinoflagellate functional diversity mediates coral survival under ecological crisis. Trends Ecol Evol 32(10):735–745
Taguchi S (1976) Relationship between photosynthesis and cell size of marine diatoms. J Phycol 12(2):185–189
Tanaka Y, Suzuki A, Sakai K (2018) The stoichiometry of coral-dinoflagellate symbiosis: carbon and nitrogen cycles are balanced in the recycling and double translocation system. ISME J 12(3):860–868
Tang EPY (1995) The allometry of algal growth rates. J Plankton Res 17(6):1325–1335
Tang EPY, Peters RH (1995) The allometry of algal respiration. J Plankton Res 17(2):303–315
Tilman D (1982) Resource competition and community structure. Princeton, Princeton University Press, p 296
Tilman D, Mattson M, Langer S (1981) Competition and nutrient kinetics along a temperature gradient: an experimental test of a mechanistic approach to niche theory. Limnol Oceanogr 26(6):1020–1033
Ulstrup KE, Ralph PJ, Larkum AWD, Kühl M (2006) Intra-colonial variability in light acclimation of zooxanthellae in coral tissues of Pocillopora damicornis. Mar Biol 149(6):1325–1335
Vásquez-Elizondo RM, Enríquez S (2017) Light absorption in coralline algae (Rhodophyta): a morphological and functional approach to understanding species distribution in a coral reef lagoon. Front Mar Sci 4:297
Violle C, Navas M, Vile D, Kazakou E, Fortunel C, Hummel I, Garnier E (2007) Let the concept of trait be functional! Oikos 116(5):882–892
Wakefield TS, Kempf SC (2001) Development of host- and symbiont-specific monoclonal antibodies and confirmation of the origin of the symbiosome membrane in a cnidarian-dinoflagellate symbiosis. Biol Bull 200(2):127–143
Warner ME, Suggett DJ (2016) The photobiology of Symbiodinium spp.: linking physiological diversity to the implications of stress and resilience. In: The Cnidaria, past, present and future, pp 489–509
Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev Camb Philos Soc 81(2):259–291
Weis VM, Davy SK, Hoegh-Guldberg O, Rodriguez-Lanetty M, Pringle JR (2008) Cell biology in model systems as the key to understanding corals. Trends Ecol Evol 23(7):369–376
Werner GDA, Cornelissen JHC, Cornwell WK, Soudzilovskaia NA, Kattge J, West SA, Kiers TE (2018) Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown. Proc Natl Acad Sci 115(20):5229–5234
Wilkerson FP, Trench RK (1986) Uptake of dissolved inorganic nitrogen by the symbiotic clam Tridacna gigas and the coral Acropora sp. Mar Biol 93(2):237–246
Wood-Charlson EM, Hollingsworth LL, Krupp DA, Weis VM (2006) Lectin/glycan interactions play a role in recognition in a coral/dinoflagellate symbiosis. Cell Microbiol 8(12):1985–1993
Zhang J, He N, Liu C, Xu L, Chen Z, Li Y, Wang R, Yu G, Sun W, Xiao C, Chen HYH, Reich PB (2020) Variation and evolution of C: N ratio among different organs enable plants to adapt to N-limited environments. Glob Change Biol 26(4):2534–2543
Zhou G, Huang H, Lian J, Zhang C, Li X (2012) Habitat correlation of Symbiodinium diversity in two reef-building coral species in an upwelling region, eastern Hainan Island, China. J Mar Biol Assoc UK 92(6):1309–1316
Ziegler M, Eguíluz VM, Duarte CM, Voolstra CR (2018) Rare symbionts may contribute to the resilience of coral-algal assemblages. ISME J 12(1):161–172
Acknowledgements
We thank David Suggett and another anonymous reviewer whose detailed comments greatly improved the manuscript. Algal cultures were provided by BURR Culture Collection, Buffalo Undersea Reef Research and maintained at the University of Hong Kong.
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This study was supported by Research Grants Council Hong Kong (GRF #17100014) awarded to DMB.
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DB conceived the ideas and secured funding; JW performed experiments and collected the data; JW and SE analyzed and interpreted the data; All authors revised, edited and approved the final manuscript and have agreed to authorship and submission of the manuscript for peer review.
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Wong, J.C.Y., Enríquez, S. & Baker, D.M. Towards a trait-based understanding of Symbiodiniaceae nutrient acquisition strategies. Coral Reefs 40, 625–639 (2021). https://doi.org/10.1007/s00338-020-02034-1
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DOI: https://doi.org/10.1007/s00338-020-02034-1